The Potential of Frog Skin Peptides for Anti-Infective Therapies: The Case of Esculentin-1a(1-21)NH2

Author(s): Bruno Casciaro*, Floriana Cappiello, Maria Rosa Loffredo, Francesca Ghirga, Maria Luisa Mangoni*

Journal Name: Current Medicinal Chemistry

Volume 27 , Issue 9 , 2020


  Journal Home
Translate in Chinese
Become EABM
Become Reviewer
Call for Editor

Abstract:

Antimicrobial Peptides (AMPs) are the key effectors of the innate immunity and represent promising molecules for the development of new antibacterial drugs. However, to achieve this goal, some problems need to be overcome: (i) the cytotoxic effects at high concentrations; (ii) the poor biostability and (iii) the difficulty in reaching the target site. Frog skin is one of the richest natural storehouses of AMPs, and over the years, many peptides have been isolated from it, characterized and classified into several families encompassing temporins, brevinins, nigrocins and esculentins. In this review, we summarized how the isolation/characterization of peptides belonging to the esculentin-1 family drove us to the design of an analogue, i.e. esculentin-1a(1-21)NH2, with a powerful antimicrobial action and immunomodulatory properties. The peptide had a wide spectrum of activity, especially against the opportunistic Gram-negative bacterium Pseudomonas aeruginosa. We described the structural features and the in vitro/in vivo biological characterization of this peptide as well as the strategies used to improve its biological properties. Among them: (i) the design of a diastereomer carrying Damino acids in order to reduce the peptide’s cytotoxicity and improve its half-life; (ii) the covalent conjugation of the peptide to gold nanoparticles or its encapsulation into poly(lactide- co-glycolide) nanoparticles; and (iii) the peptide immobilization to biomedical devices (such as silicon hydrogel contact lenses) to obtain an antibacterial surface able to reduce microbial growth and attachment. Summing up the best results obtained so far, this review traces all the steps that led these frog-skin AMPs to the direction of peptide-based drugs for clinical use.

Keywords: Antimicrobial peptides, Pseudomonas aeruginosa, innate immunity, gold nanoparticles, contact lenses, D-amino acids, wound healing.

[1]
Boto, A.; Pérez de la Lastra, J.M.; González, C.C. The road from host-defense peptides to a new generation of antimicrobial drugs. Molecules, 2018, 23(2), E311
[http://dx.doi.org/10.3390/molecules23020311] [PMID: 29389911]
[2]
Ageitos, J.M.; Sánchez-Pérez, A.; Calo-Mata, P.; Villa, T.G. Antimicrobial peptides (AMPs): Ancient compounds that represent novel weapons in the fight against bacteria. Biochem. Pharmacol., 2017, 133, 117-138.
[http://dx.doi.org/10.1016/j.bcp.2016.09.018] [PMID: 27663838]
[3]
Maróti, G.; Kereszt, A.; Kondorosi, E.; Mergaert, P. Natural roles of antimicrobial peptides in microbes, plants and animals. Res. Microbiol., 2011, 162(4), 363-374.
[http://dx.doi.org/10.1016/j.resmic.2011.02.005] [PMID: 21320593]
[4]
Tang, S.S.; Prodhan, Z.H.; Biswas, S.K.; Le, C.F.; Sekaran, S.D. Antimicrobial peptides from different plant sources: Isolation, characterisation, and purification. Phytochemistry, 2018, 154, 94-105.
[http://dx.doi.org/10.1016/j.phytochem.2018.07.002] [PMID: 30031244]
[5]
Faye, I.; Lindberg, B.G. Towards a paradigm shift in innate immunity-seminal work by Hans G. Boman and co-workers. Philos. Trans. R. Soc. Lond. B Biol. Sci., 2016, 371(1695), 371.
[http://dx.doi.org/10.1098/rstb.2015.0303] [PMID: 27160604]
[6]
Lehrer, R.I. Primate defensins. Nat. Rev. Microbiol., 2004, 2(9), 727-738.
[http://dx.doi.org/10.1038/nrmicro976] [PMID: 15372083]
[7]
Berkowitz, B.A.; Bevins, C.L.; Zasloff, M.A. Magainins: a new family of membrane-active host defense peptides. Biochem. Pharmacol., 1990, 39(4), 625-629.
[http://dx.doi.org/10.1016/0006-2952(90)90138-B] [PMID: 1689576]
[8]
Steckbeck, J.D.; Deslouches, B.; Montelaro, R.C. Antimicrobial peptides: new drugs for bad bugs? Expert Opin. Biol. Ther., 2014, 14(1), 11-14.
[http://dx.doi.org/10.1517/14712598.2013.844227] [PMID: 24206062]
[9]
Sharma, K.; Aaghaz, S.; Shenmar, K.; Jain, R. Short antimicrobial peptides. Recent Pat Antiinfect Drug Discov, 2018, 13(1), 12-52.
[http://dx.doi.org/10.2174/1574891X13666180628105928] [PMID: 29952266]
[10]
Pasupuleti, M.; Schmidtchen, A.; Malmsten, M. Antimicrobial peptides: key components of the innate immune system. Crit. Rev. Biotechnol., 2012, 32(2), 143-171.
[http://dx.doi.org/10.3109/07388551.2011.594423] [PMID: 22074402]
[11]
Ganz, T. Defensins: antimicrobial peptides of innate immunity. Nat. Rev. Immunol., 2003, 3(9), 710-720.
[http://dx.doi.org/10.1038/nri1180] [PMID: 12949495]
[12]
Brogden, K.A.; Ackermann, M.; McCray, P.B. Jr.; Tack, B.F. Antimicrobial peptides in animals and their role in host defences. Int. J. Antimicrob. Agents, 2003, 22(5), 465-478.
[http://dx.doi.org/10.1016/S0924-8579(03)00180-8] [PMID: 14602364]
[13]
Boman, H.G. Antibacterial peptides: key components needed in immunity. Cell, 1991, 65(2), 205-207.
[http://dx.doi.org/10.1016/0092-8674(91)90154-Q] [PMID: 2015623]
[14]
Hancock, R.E.; Diamond, G. The role of cationic antimicrobial peptides in innate host defences. Trends Microbiol., 2000, 8(9), 402-410.
[http://dx.doi.org/10.1016/S0966-842X(00)01823-0] [PMID: 10989307]
[15]
Zasloff, M. Antimicrobial peptides of multicellular organisms. Nature, 2002, 415(6870), 389-395.
[http://dx.doi.org/10.1038/415389a] [PMID: 11807545]
[16]
Mangoni, M.L.; McDermott, A.M.; Zasloff, M. Antimicrobial peptides and wound healing: biological and therapeutic considerations. Exp. Dermatol., 2016, 25(3), 167-173.
[http://dx.doi.org/10.1111/exd.12929] [PMID: 26738772]
[17]
Bals, R. Epithelial antimicrobial peptides in host defense against infection. Respir. Res., 2000, 1(3), 141-150.
[http://dx.doi.org/10.1186/rr25] [PMID: 11667978]
[18]
Huang, H.W.; Charron, N.E. Understanding membrane-active antimicrobial peptides. Q. Rev. Biophys., 2017, 50e10
[http://dx.doi.org/10.1017/S0033583517000087] [PMID: 29233222]
[19]
Mangoni, M.L.; Papo, N.; Saugar, J.M.; Barra, D.; Shai, Y.; Simmaco, M.; Rivas, L. Effect of natural L- to D-amino acid conversion on the organization, membrane binding, and biological function of the antimicrobial peptides bombinins H. Biochemistry, 2006, 45(13), 4266-4276.
[http://dx.doi.org/10.1021/bi052150y] [PMID: 16566601]
[20]
Nicolas, P.; El Amri, C. The dermaseptin superfamily: a gene-based combinatorial library of antimicrobial peptides. Biochim. Biophys. Acta, 2009, 1788(8), 1537-1550.
[http://dx.doi.org/10.1016/j.bbamem.2008.09.006] [PMID: 18929530]
[21]
Wang, G. Post-translational modifications of natural antimicrobial peptides and strategies for peptide engineering. Curr. Biotechnol., 2012, 1(1), 72-79.
[http://dx.doi.org/10.2174/2211550111201010072] [PMID: 24511461]
[22]
Thaiss, C.A.; Levy, M.; Itav, S.; Elinav, E. Integration of innate immune signaling. Trends Immunol., 2016, 37(2), 84-101.
[http://dx.doi.org/10.1016/j.it.2015.12.003] [PMID: 26755064]
[23]
Hemshekhar, M.; Anaparti, V.; Mookherjee, N. Functions of cationic host defense peptides in immunity. Pharmaceuticals (Basel), 2016, 9(3), E40
[http://dx.doi.org/10.3390/ph9030040] [PMID: 27384571]
[24]
Davidson, D.J.; Currie, A.J.; Reid, G.S.; Bowdish, D.M.; MacDonald, K.L.; Ma, R.C.; Hancock, R.E.; Speert, D.P. The cationic antimicrobial peptide LL-37 modulates dendritic cell differentiation and dendritic cell-induced T cell polarization. J. Immunol., 2004, 172(2), 1146-1156.
[http://dx.doi.org/10.4049/jimmunol.172.2.1146] [PMID: 14707090]
[25]
Afacan, N.J.; Yeung, A.T.; Pena, O.M.; Hancock, R.E. Therapeutic potential of host defense peptides in antibiotic-resistant infections. Curr. Pharm. Des., 2012, 18(6), 807-819.
[http://dx.doi.org/10.2174/138161212799277617] [PMID: 22236127]
[26]
Mookherjee, N.; Hancock, R.E. Cationic host defence peptides: innate immune regulatory peptides as a novel approach for treating infections. Cell. Mol. Life Sci., 2007, 64(7-8), 922-933.
[http://dx.doi.org/10.1007/s00018-007-6475-6] [PMID: 17310278]
[27]
Rinaldi, A.C. Antimicrobial peptides from amphibian skin: an expanding scenario. Curr. Opin. Chem. Biol., 2002, 6(6), 799-804.
[http://dx.doi.org/10.1016/S1367-5931(02)00401-5] [PMID: 12470734]
[28]
Hancock, R.E.; Sahl, H.G. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol., 2006, 24(12), 1551-1557.
[http://dx.doi.org/10.1038/nbt1267] [PMID: 17160061]
[29]
Powers, J.P.; Hancock, R.E. The relationship between peptide structure and antibacterial activity. Peptides, 2003, 24(11), 1681-1691.
[http://dx.doi.org/10.1016/j.peptides.2003.08.023] [PMID: 15019199]
[30]
Mojsoska, B.; Jenssen, H. Peptides and peptidomimetics for antimicrobial drug design. Pharmaceuticals (Basel), 2015, 8(3), 366-415.
[http://dx.doi.org/10.3390/ph8030366] [PMID: 26184232]
[31]
Mahlapuu, M.; Håkansson, J.; Ringstad, L.; Björn, C. Antimicrobial peptides: an emerging category of therapeutic agents. Front. Cell. Infect. Microbiol., 2016, 6, 194.
[http://dx.doi.org/10.3389/fcimb.2016.00194] [PMID: 28083516]
[32]
Hall, K.; Aguilar, M.I. Surface plasmon resonance spectroscopy for studying the membrane binding of antimicrobial peptides. Methods Mol. Biol., 2010, 627, 213-223.
[http://dx.doi.org/10.1007/978-1-60761-670-2_14] [PMID: 20217624]
[33]
Ehrenstein, G.; Lecar, H. Electrically gated ionic channels in lipid bilayers. Q. Rev. Biophys., 1977, 10(1), 1-34.
[http://dx.doi.org/10.1017/S0033583500000123] [PMID: 327501]
[34]
Zhang, L.; Rozek, A.; Hancock, R.E. Interaction of cationic antimicrobial peptides with model membranes. J. Biol. Chem., 2001, 276(38), 35714-35722.
[http://dx.doi.org/10.1074/jbc.M104925200] [PMID: 11473117]
[35]
Brogden, K.A. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol., 2005, 3(3), 238-250.
[http://dx.doi.org/10.1038/nrmicro1098] [PMID: 15703760]
[36]
Shai, Y. Mode of action of membrane active antimicrobial peptides. Biopolymers, 2002, 66(4), 236-248.
[http://dx.doi.org/10.1002/bip.10260] [PMID: 12491537]
[37]
Bechinger, B.; Gorr, S.U. Antimicrobial peptides: mechanisms of action and resistance. J. Dent. Res., 2017, 96(3), 254-260.
[http://dx.doi.org/10.1177/0022034516679973] [PMID: 27872334]
[38]
Conlon, J.M. Structural diversity and species distribution of host-defense peptides in frog skin secretions. Cell. Mol. Life Sci., 2011, 68(13), 2303-2315.
[http://dx.doi.org/10.1007/s00018-011-0720-8] [PMID: 21560068]
[39]
Wang, G.; Li, X.; Wang, Z. APD3: the antimicrobial peptide database as a tool for research and education. Nucleic Acids Res., 2016, 44(D1), D1087-D1093.
[http://dx.doi.org/10.1093/nar/gkv1278] [PMID: 26602694]
[40]
Xu, X.; Lai, R. The chemistry and biological activities of peptides from amphibian skin secretions. Chem. Rev., 2015, 115(4), 1760-1846.
[http://dx.doi.org/10.1021/cr4006704] [PMID: 25594509]
[41]
Mangoni, M.L. Temporins, anti-infective peptides with expanding properties. Cell. Mol. Life Sci., 2006, 63(9), 1060-1069.
[http://dx.doi.org/10.1007/s00018-005-5536-y] [PMID: 16572270]
[42]
Conlon, J.M. The contribution of skin antimicrobial peptides to the system of innate immunity in anurans. Cell Tissue Res., 2011, 343(1), 201-212.
[http://dx.doi.org/10.1007/s00441-010-1014-4] [PMID: 20640445]
[43]
Conlon, J.M.; Kolodziejek, J.; Nowotny, N. Antimicrobial peptides from the skins of North American frogs. Biochim. Biophys. Acta, 2009, 1788(8), 1556-1563.
[http://dx.doi.org/10.1016/j.bbamem.2008.09.018] [PMID: 18983817]
[44]
Pantic, J.M.; Jovanovic, I.P.; Radosavljevic, G.D.; Arsenijevic, N.N.; Conlon, J.M.; Lukic, M.L. The potential of frog skin-derived peptides for development into therapeutically-valuable immunomodulatory agents. Molecules, 2017, 22(12), E2071
[http://dx.doi.org/10.3390/molecules22122071] [PMID: 29236056]
[45]
Park, J.M.; Jung, J.E.; Lee, B.J. Antimicrobial peptides from the skin of a Korean frog, Rana rugosa. Biochem. Biophys. Res. Commun., 1995, 209(2), 775.
[http://dx.doi.org/10.1006/bbrc.1995.1567] [PMID: 7733950]
[46]
Conlon, J.M.; Kolodziejek, J.; Nowotny, N. Antimicrobial peptides from ranid frogs: taxonomic and phylogenetic markers and a potential source of new therapeutic agents. Biochim. Biophys. Acta, 2004, 1696(1), 1-14.
[http://dx.doi.org/10.1016/j.bbapap.2003.09.004] [PMID: 14726199]
[47]
Matutte, B.; Storey, K.B.; Knoop, F.C.; Conlon, J.M. Induction of synthesis of an antimicrobial peptide in the skin of the freeze-tolerant frog, Rana sylvatica, in response to environmental stimuli. FEBS Lett., 2000, 483(2-3), 135-138.
[http://dx.doi.org/10.1016/S0014-5793(00)02102-5] [PMID: 11042268]
[48]
Yan, H.; Hancock, R.E. Synergistic interactions between mammalian antimicrobial defense peptides. Antimicrob. Agents Chemother., 2001, 45(5), 1558-1560.
[http://dx.doi.org/10.1128/AAC.45.5.1558-1560.2001] [PMID: 11302828]
[49]
Rosenfeld, Y.; Barra, D.; Simmaco, M.; Shai, Y.; Mangoni, M.L. A synergism between temporins toward Gram-negative bacteria overcomes resistance imposed by the lipopolysaccharide protective layer. J. Biol. Chem., 2006, 281(39), 28565-28574.
[http://dx.doi.org/10.1074/jbc.M606031200] [PMID: 16867990]
[50]
Merlino, F.; Carotenuto, A.; Casciaro, B.; Martora, F.; Loffredo, M.R.; Di Grazia, A.; Yousif, A.M.; Brancaccio, D.; Palomba, L.; Novellino, E.; Galdiero, M.; Iovene, M.R.; Mangoni, M.L.; Grieco, P. Glycine-replaced derivatives of [Pro3,DLeu9]TL, a temporin L analogue: Evaluation of antimicrobial, cytotoxic and hemolytic activities. Eur. J. Med. Chem., 2017, 139, 750-761.
[http://dx.doi.org/10.1016/j.ejmech.2017.08.040] [PMID: 28863356]
[51]
Mangoni, M.L.; Grazia, A.D.; Cappiello, F.; Casciaro, B.; Luca, V. Naturally occurring peptides from Rana temporaria: Antimicrobial properties and more. Curr. Top. Med. Chem., 2016, 16(1), 54-64.
[http://dx.doi.org/10.2174/1568026615666150703121403] [PMID: 26139114]
[52]
Musale, V.; Casciaro, B.; Mangoni, M.L.; Abdel-Wahab, Y.H.A.; Flatt, P.R.; Conlon, J.M. Assessment of the potential of temporin peptides from the frog Rana temporaria (Ranidae) as anti-diabetic agents. J. Pept. Sci., 2018, 24(2)
[http://dx.doi.org/10.1002/psc.3065] [PMID: 29349894]
[53]
Marcocci, M.E.; Amatore, D.; Villa, S.; Casciaro, B.; Aimola, P.; Franci, G.; Grieco, P.; Galdiero, M.; Palamara, A.T.; Mangoni, M.L.; Nencioni, L. The amphibian antimicrobial peptide temporin B inhibits in vitro herpes simplex virus 1 infection. Antimicrob. Agents Chemother., 2018, 62(5), e02367
[http://dx.doi.org/10.1128/AAC.02367-17] [PMID: 29483113]
[54]
Musale, V.; Abdel-Wahab, Y.H.A.; Flatt, P.R.; Conlon, J.M.; Mangoni, M.L. Insulinotropic, glucose-lowering, and beta-cell anti-apoptotic actions of peptides related to esculentin-1a(1-21).NH2. Amino Acids, 2018, 50(6), 723-734.
[http://dx.doi.org/10.1007/s00726-018-2551-5] [PMID: 29549522]
[55]
Conlon, J.M. Reflections on a systematic nomenclature for antimicrobial peptides from the skins of frogs of the family Ranidae. Peptides, 2008, 29(10), 1815-1819.
[http://dx.doi.org/10.1016/j.peptides.2008.05.029] [PMID: 18585417]
[56]
Basir, Y.J.; Knoop, F.C.; Dulka, J.; Conlon, J.M. Multiple antimicrobial peptides and peptides related to bradykinin and neuromedin N isolated from skin secretions of the pickerel frog, Rana palustris. Biochim. Biophys. Acta, 2000, 1543(1), 95-105.
[http://dx.doi.org/10.1016/S0167-4838(00)00191-6] [PMID: 11087945]
[57]
Ali, M.F.; Lips, K.R.; Knoop, F.C.; Fritzsch, B.; Miller, C.; Conlon, J.M. Antimicrobial peptides and protease inhibitors in the skin secretions of the crawfish frog, Rana areolata. Biochim. Biophys. Acta, 2002, 1601(1), 55-63.
[http://dx.doi.org/10.1016/S1570-9639(02)00432-6] [PMID: 12429503]
[58]
Wang, H.; Yu, Z.; Hu, Y.; Yu, H.; Ran, R.; Xia, J.; Wang, D.; Yang, S.; Yang, X.; Liu, J. Molecular cloning and characterization of antimicrobial peptides from skin of the broad-folded frog, Hylarana latouchii. Biochimie, 2012, 94(6), 1317-1326.
[http://dx.doi.org/10.1016/j.biochi.2012.02.032] [PMID: 22426384]
[59]
Li, J.; Xu, X.; Xu, C.; Zhou, W.; Zhang, K.; Yu, H.; Zhang, Y.; Zheng, Y.; Rees, H.H.; Lai, R.; Yang, D.; Wu, J. Anti-infection peptidomics of amphibian skin. Mol. Cell. Proteomics, 2007, 6(5), 882-894.
[http://dx.doi.org/10.1074/mcp.M600334-MCP200] [PMID: 17272268]
[60]
Iwakoshi-Ukena, E.; Ukena, K.; Okimoto, A.; Soga, M.; Okada, G.; Sano, N.; Fujii, T.; Sugawara, Y.; Sumida, M. Identification and characterization of antimicrobial peptides from the skin of the endangered frog Odorrana ishikawae. Peptides, 2011, 32(4), 670-676.
[http://dx.doi.org/10.1016/j.peptides.2010.12.013] [PMID: 21193000]
[61]
Marenah, L.; Flatt, P.R.; Orr, D.F.; Shaw, C.; Abdel-Wahab, Y.H. Skin secretions of Rana saharica frogs reveal antimicrobial peptides esculentins-1 and -1B and brevinins-1E and -2EC with novel insulin releasing activity. J. Endocrinol., 2006, 188(1), 1-9.
[http://dx.doi.org/10.1677/joe.1.06293] [PMID: 16394170]
[62]
Conlon, J.M.; Meetani, M.A.; Coquet, L.; Jouenne, T.; Leprince, J.; Vaudry, H.; Kolodziejek, J.; Nowotny, N.; King, J.D. Antimicrobial peptides from the skin secretions of the New World frogs Lithobates capito and Lithobates warszewitschii (Ranidae). Peptides, 2009, 30(10), 1775-1781.
[http://dx.doi.org/10.1016/j.peptides.2009.07.011] [PMID: 19635516]
[63]
Conlon, J.M.; Kolodziejek, J.; Mechkarska, M.; Coquet, L.; Leprince, J.; Jouenne, T.; Vaudry, H.; Nielsen, P.F.; Nowotny, N.; King, J.D. Host defense peptides from Lithobates forreri, Hylarana luctuosa, and Hylarana signata (Ranidae): phylogenetic relationships inferred from primary structures of ranatuerin-2 and brevinin-2 peptides. Comp. Biochem. Physiol. Part D Genomics Proteomics, 2014, 9, 49-57.
[http://dx.doi.org/10.1016/j.cbd.2014.01.002] [PMID: 24463457]
[64]
Simmaco, M.; Mignogna, G.; Barra, D.; Bossa, F. Novel antimicrobial peptides from skin secretion of the European frog Rana esculenta. FEBS Lett., 1993, 324(2), 159-161.
[http://dx.doi.org/10.1016/0014-5793(93)81384-C] [PMID: 8508915]
[65]
Simmaco, M.; Mignogna, G.; Barra, D.; Bossa, F. Antimicrobial peptides from skin secretions of Rana esculenta. Molecular cloning of cDNAs encoding esculentin and brevinins and isolation of new active peptides. J. Biol. Chem., 1994, 269(16), 11956-11961.
[PMID: 8163497]
[66]
Wang, Y.; Zhang, Y.; Lee, W.H.; Yang, X.; Zhang, Y. Novel peptides from skins of amphibians showed broad-spectrum antimicrobial activities. Chem. Biol. Drug Des., 2016, 87(3), 419-424.
[http://dx.doi.org/10.1111/cbdd.12672] [PMID: 26452973]
[67]
Ponti, D.; Mignogna, G.; Mangoni, M.L.; De Biase, D.; Simmaco, M.; Barra, D. Expression and activity of cyclic and linear analogues of esculentin-1, an anti-microbial peptide from amphibian skin. Eur. J. Biochem., 1999, 263(3), 921-927.
[http://dx.doi.org/10.1046/j.1432-1327.1999.00597.x] [PMID: 10469159]
[68]
Segura, A.; Moreno, M.; Molina, A.; García-Olmedo, F. Novel defensin subfamily from spinach (Spinacia oleracea). FEBS Lett., 1998, 435(2-3), 159-162.
[http://dx.doi.org/10.1016/S0014-5793(98)01060-6] [PMID: 9762899]
[69]
Ponti, D.; Mangoni, M.L.; Mignogna, G.; Simmaco, M.; Barra, D. An amphibian antimicrobial peptide variant expressed in Nicotiana tabacum confers resistance to phytopathogens. Biochem. J., 2003, 370(Pt 1), 121-127.
[http://dx.doi.org/10.1042/bj20021444] [PMID: 12435273]
[70]
Orivel, J.; Redeker, V.; Le Caer, J.P.; Krier, F.; Revol-Junelles, A.M.; Longeon, A.; Chaffotte, A.; Dejean, A.; Rossier, J. Ponericins, new antibacterial and insecticidal peptides from the venom of the ant Pachycondyla goeldii. J. Biol. Chem., 2001, 276(21), 17823-17829.
[http://dx.doi.org/10.1074/jbc.M100216200] [PMID: 11279030]
[71]
Mangoni, M.L.; Fiocco, D.; Mignogna, G.; Barra, D.; Simmaco, M. Functional characterisation of the 1-18 fragment of esculentin-1b, an antimicrobial peptide from Rana esculenta. Peptides, 2003, 24(11), 1771-1777.
[http://dx.doi.org/10.1016/j.peptides.2003.07.029] [PMID: 15019209]
[72]
Islas-Rodrìguez, A.E.; Marcellini, L.; Orioni, B.; Barra, D.; Stella, L.; Mangoni, M.L. Esculentin 1-21: a linear antimicrobial peptide from frog skin with inhibitory effect on bovine mastitis-causing bacteria. J. Pept. Sci., 2009, 15(9), 607-614.
[http://dx.doi.org/10.1002/psc.1148] [PMID: 19507197]
[73]
Loffredo, M.R.; Ghosh, A.; Harmouche, N.; Casciaro, B.; Luca, V.; Bortolotti, A.; Cappiello, F.; Stella, L.; Bhunia, A.; Bechinger, B.; Mangoni, M.L. Membrane perturbing activities and structural properties of the frog-skin derived peptide Esculentin-1a(1-21)NH2 and its Diastereomer Esc(1-21)-1c: Correlation with their antipseudomonal and cytotoxic activity. Biochim. Biophys. Acta Biomembr., 2017, 1859(12), 2327-2339.
[http://dx.doi.org/10.1016/j.bbamem.2017.09.009] [PMID: 28912103]
[74]
Di Grazia, A.; Cappiello, F.; Cohen, H.; Casciaro, B.; Luca, V.; Pini, A.; Di, Y.P.; Shai, Y.; Mangoni, M.L. D-Amino acids incorporation in the frog skin-derived peptide esculentin-1a(1-21)NH2 is beneficial for its multiple functions. Amino Acids, 2015, 47(12), 2505-2519.
[http://dx.doi.org/10.1007/s00726-015-2041-y] [PMID: 26162435]
[75]
Klaas, I.C.; Zadoks, R.N. An update on environmental mastitis: Challenging perceptions. Transbound. Emerg. Dis., 2018, 65(Suppl. 1), 166-185.
[http://dx.doi.org/10.1111/tbed.12704] [PMID: 29083115]
[76]
Luca, V.; Stringaro, A.; Colone, M.; Pini, A.; Mangoni, M.L. Esculentin(1-21), an amphibian skin membrane-active peptide with potent activity on both planktonic and biofilm cells of the bacterial pathogen Pseudomonas aeruginosa. Cell. Mol. Life Sci., 2013, 70(15), 2773-2786.
[http://dx.doi.org/10.1007/s00018-013-1291-7] [PMID: 23503622]
[77]
Parkins, M.D.; Somayaji, R.; Waters, V.J. Epidemiology, biology, and impact of clonal Pseudomonas aeruginosa infections in cystic fibrosis. Clin. Microbiol. Rev., 2018, 31(4), e00019-e18.
[http://dx.doi.org/10.1128/CMR.00019-18] [PMID: 30158299]
[78]
Cappiello, F.; Casciaro, B.; Mangoni, M.L. A novel in vitro wound healing assay to evaluate cell migration. J. Vis. Exp., 2018, (133)
[http://dx.doi.org/10.3791/56825] [PMID: 29608162]
[79]
Cappiello, F.; Di Grazia, A.; Segev-Zarko, L.A.; Scali, S.; Ferrera, L.; Galietta, L.; Pini, A.; Shai, Y.; Di, Y.P.; Mangoni, M.L. Esculentin-1a-derived peptides promote clearance of Pseudomonas aeruginosa internalized in bronchial cells of cystic fibrosis patients and lung cell migration: biochemical properties and a plausible mode of action. Antimicrob. Agents Chemother., 2016, 60(12), 7252-7262.
[http://dx.doi.org/10.1128/AAC.00904-16] [PMID: 27671059]
[80]
Kolar, S.S.N.; Luca, V.; Baidouri, H.; Mannino, G.; McDermott, A.M.; Mangoni, M.L. Esculentin-1a(1-21)NH2: a frog skin-derived peptide for microbial keratitis. Cell. Mol. Life Sci., 2015, 72(3), 617-627.
[http://dx.doi.org/10.1007/s00018-014-1694-0] [PMID: 25086859]
[81]
Casciaro, B.; Cappiello, F.; Cacciafesta, M.; Mangoni, M.L. Promising approaches to optimize the biological properties of the antimicrobial peptide Esculentin-1a(1-21)Nh2: amino acids substitution and conjugation to nanoparticles. Front Chem., 2017, 5, 26.
[http://dx.doi.org/10.3389/fchem.2017.00026] [PMID: 28487853]
[82]
Jia, F.; Wang, J.; Peng, J.; Zhao, P.; Kong, Z.; Wang, K.; Yan, W.; Wang, R. D-amino acid substitution enhances the stability of antimicrobial peptide polybia-CP. Acta Biochim. Biophys. Sin. (Shanghai), 2017, 49(10), 916-925.
[http://dx.doi.org/10.1093/abbs/gmx091] [PMID: 28981608]
[83]
Saint Jean, K.D.; Henderson, K.D.; Chrom, C.L.; Abiuso, L.E.; Renn, L.M.; Caputo, G.A. Effects of hydrophobic amino acid substitutions on antimicrobial peptide behavior. Probiotics Antimicrob. Proteins, 2018, 10(3), 408-419.
[http://dx.doi.org/10.1007/s12602-017-9345-z] [PMID: 29103131]
[84]
Junior, E.F.C.; Guimarães, C.F.R.C.; Franco, L.L.; Alves, R.J.; Kato, K.C.; Martins, H.R.; de Souza Filho, J.D.; Bemquerer, M.P.; Munhoz, V.H.O.; Resende, J.M.; Verly, R.M. Glycotriazole-peptides derived from the peptide HSP1: synergistic effect of triazole and saccharide rings on the antifungal activity. Amino Acids, 2017, 49(8), 1389-1400.
[http://dx.doi.org/10.1007/s00726-017-2441-2] [PMID: 28573520]
[85]
Albada, H.B.; Prochnow, P.; Bobersky, S.; Langklotz, S.; Schriek, P.; Bandow, J.E.; Metzler-Nolte, N. Tuning the activity of a short arg-trp antimicrobial Peptide by lipidation of a C- or N-terminal lysine side-chain. ACS Med. Chem. Lett., 2012, 3(12), 980-984.
[http://dx.doi.org/10.1021/ml300148v] [PMID: 24900420]
[86]
Zhang, S.K.; Song, J.W.; Gong, F.; Li, S.B.; Chang, H.Y.; Xie, H.M.; Gao, H.W.; Tan, Y.X.; Ji, S.P. Design of an α-helical antimicrobial peptide with improved cell-selective and potent anti-biofilm activity. Sci. Rep., 2016, 6, 27394.
[http://dx.doi.org/10.1038/srep27394] [PMID: 27271216]
[87]
Huang, Y.; He, L.; Li, G.; Zhai, N.; Jiang, H.; Chen, Y. Role of helicity of α-helical antimicrobial peptides to improve specificity. Protein Cell, 2014, 5(8), 631-642.
[http://dx.doi.org/10.1007/s13238-014-0061-0] [PMID: 24805306]
[88]
Biondi, B.; Casciaro, B.; Di Grazia, A.; Cappiello, F.; Luca, V.; Crisma, M.; Mangoni, M.L. Effects of Aib residues insertion on the structural-functional properties of the frog skin-derived peptide esculentin-1a(1-21)NH2. Amino Acids, 2017, 49(1), 139-150.
[http://dx.doi.org/10.1007/s00726-016-2341-x] [PMID: 27726008]
[89]
Buommino, E.; Carotenuto, A.; Antignano, I.; Bellavita, R.; Casciaro, B.; Loffredo, M.R.; Merlino, F.; Novellino, E.; Mangoni, M.L.; Nocera, F.P.; Brancaccio, D.; Punzi, P.; Roversi, D.; Ingenito, R.; Bianchi, E.; Grieco, P. The Outcomes of decorated prolines in the discovery of antimicrobial peptides from Temporin-L. ChemMedChem, 2019, 14(13), 1283-1290.
[http://dx.doi.org/10.1002/cmdc.201900221] [PMID: 31087626]
[90]
Izadpanah, M.; Khalili, H. Antibiotic regimens for treatment of infections due to multidrug-resistant Gram-negative pathogens: An evidence-based literature review. J. Res. Pharm. Pract., 2015, 4(3), 105-114.
[http://dx.doi.org/10.4103/2279-042X.162360] [PMID: 26312249]
[91]
Casciaro, B.; Loffredo, M.R.; Luca, V.; Verrusio, W.; Cacciafesta, M.; Mangoni, M.L. Esculentin-1a derived antipseudomonal peptides: limited induction of resistance and synergy with aztreonam. Protein Pept. Lett., 2018, 25(12), 1155-1162.
[http://dx.doi.org/10.2174/0929866525666181101104649] [PMID: 30381056]
[92]
Davies, J.; Spiegelman, G.B.; Yim, G. The world of subinhibitory antibiotic concentrations. Curr. Opin. Microbiol., 2006, 9(5), 445-453.
[http://dx.doi.org/10.1016/j.mib.2006.08.006] [PMID: 16942902]
[93]
Andersson, D.I.; Hughes, D. Microbiological effects of sublethal levels of antibiotics. Nat. Rev. Microbiol., 2014, 12(7), 465-478.
[http://dx.doi.org/10.1038/nrmicro3270] [PMID: 24861036]
[94]
Kaplan, J.B. Antibiotic-induced biofilm formation. Int. J. Artif. Organs, 2011, 34(9), 737-751.
[http://dx.doi.org/10.5301/ijao.5000027] [PMID: 22094552]
[95]
Berditsch, M.; Afonin, S.; Vladimirova, T.; Wadhwani, P.; Ulrich, A.S. Antimicrobial peptides can enhance the risk of persistent infections. Front. Immunol., 2012, 3, 222.
[http://dx.doi.org/10.3389/fimmu.2012.00222] [PMID: 22870073]
[96]
Casciaro, B.; Lin, Q.; Afonin, S.; Loffredo, M.R.; de Turris, V.; Middel, V.; Ulrich, A.S.; Di, Y.P.; Mangoni, M.L. Inhibition of Pseudomonas aeruginosa biofilm formation and expression of virulence genes by selective epimerization in the peptide Esculentin-1a(1-21)NH2. FEBS J., 2019, 286(19), 3874-3891.
[http://dx.doi.org/10.1111/febs.14940] [PMID: 31144441]
[97]
Peschel, A.; Sahl, H.G. The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat. Rev. Microbiol., 2006, 4(7), 529-536.
[http://dx.doi.org/10.1038/nrmicro1441] [PMID: 16778838]
[98]
Hong, J.; Hu, J.; Ke, F. experimental induction of bacterial resistance to the antimicrobial peptide Tachyplesin I and investigation of the resistance mechanisms. Antimicrob. Agents Chemother., 2016, 60(10), 6067-6075.
[http://dx.doi.org/10.1128/AAC.00640-16] [PMID: 27480861]
[99]
St Helen, G.; Holland, N.T.; Balmes, J.R.; Hall, D.B.; Bernert, J.T.; Vena, J.E.; Wang, J.S.; Naeher, L.P. Utility of urinary Clara cell protein (CC16) to demonstrate increased lung epithelial permeability in non-smokers exposed to outdoor secondhand smoke. J. Expo. Sci. Environ. Epidemiol., 2013, 23(2), 183-189.
[http://dx.doi.org/10.1038/jes.2012.68] [PMID: 22805990]
[100]
Chen, C.; Mangoni, M.L.; Di, Y.P. In vivo therapeutic efficacy of frog skin-derived peptides against Pseudomonas aeruginosa-induced pulmonary infection. Sci. Rep., 2017, 7(1), 8548.
[http://dx.doi.org/10.1038/s41598-017-08361-8] [PMID: 28819175]
[101]
Rai, A.; Pinto, S.; Velho, T.R.; Ferreira, A.F.; Moita, C.; Trivedi, U.; Evangelista, M.; Comune, M.; Rumbaugh, K.P.; Simões, P.N.; Moita, L.; Ferreira, L. One-step synthesis of high-density peptide-conjugated gold nanoparticles with antimicrobial efficacy in a systemic infection model. Biomaterials, 2016, 85, 99-110.
[http://dx.doi.org/10.1016/j.biomaterials.2016.01.051] [PMID: 26866877]
[102]
Torres, L.M.F.C.; Almeida, M.T.; Santos, T.L.; Marinho, L.E.S.; de Mesquita, J.P.; da Silva, L.M.; Dos Santos, W.T.P.; Martins, H.R.; Kato, K.C.; Alves, E.S.F.; Liao, L.M.; de Magalhães, M.T.Q.; de Mendonça, F.G.; Pereira, F.V.; Resende, J.M.; Bemquerer, M.P.; Rodrigues, M.A.; Verly, R.M. Antimicrobial alumina nanobiostructures of disulfide- and triazole-linked peptides: Synthesis, characterization, membrane interactions and biological activity. Colloids Surf. B Biointerfaces, 2019, 177, 94-104.
[http://dx.doi.org/10.1016/j.colsurfb.2019.01.052] [PMID: 30711763]
[103]
Dutta, D.; Willcox, M.D. Antimicrobial contact lenses and lens cases: a review. Eye Contact Lens, 2014, 40(5), 312-324.
[http://dx.doi.org/10.1097/ICL.0000000000000056] [PMID: 25083781]
[104]
Kamaruzzaman, N.F.; Tan, L.P.; Hamdan, R.H.; Choong, S.S.; Wong, W.K.; Gibson, A.J.; Chivu, A.; Pina, M.F. Antimicrobial polymers: the potential replacement of existing antibiotics? Int. J. Mol. Sci., 2019, 20(11), E2747
[http://dx.doi.org/10.3390/ijms20112747] [PMID: 31167476]
[105]
Elahi, N.; Kamali, M.; Baghersad, M.H. Recent biomedical applications of gold nanoparticles: A review. Talanta, 2018, 184, 537-556.
[http://dx.doi.org/10.1016/j.talanta.2018.02.088] [PMID: 29674080]
[106]
Casciaro, B.; Moros, M.; Rivera-Fernández, S.; Bellelli, A.; de la Fuente, J.M.; Mangoni, M.L. Gold-nanoparticles coated with the antimicrobial peptide esculentin-1a(1-21)NH2 as a reliable strategy for antipseudomonal drugs. Acta Biomater., 2017, 47, 170-181.
[http://dx.doi.org/10.1016/j.actbio.2016.09.041] [PMID: 27693686]
[107]
Ciofu, O.; Tolker-Nielsen, T. Tolerance and resistance of Pseudomonas aeruginosa biofilms to antimicrobial agents-How P. aeruginosa Can Escape Antibiotics. Front. Microbiol., 2019, 10, 913.
[http://dx.doi.org/10.3389/fmicb.2019.00913] [PMID: 31130925]
[108]
d’Angelo, I.; Casciaro, B.; Miro, A.; Quaglia, F.; Mangoni, M.L.; Ungaro, F. Overcoming barriers in Pseudomonas aeruginosa lung infections: Engineered nanoparticles for local delivery of a cationic antimicrobial peptide. Colloids Surf. B Biointerfaces, 2015, 135, 717-725.
[http://dx.doi.org/10.1016/j.colsurfb.2015.08.027] [PMID: 26340361]
[109]
d’Angelo, I.; Quaglia, F.; Ungaro, F. PLGA carriers for inhalation: where do we stand, where are we headed? Ther. Deliv., 2015, 6(10), 1139-1144.
[http://dx.doi.org/10.4155/tde.15.37] [PMID: 26606854]
[110]
Debnath, S.K.; Saisivam, S.; Omri, A. PLGA Ethionamide Nanoparticles for Pulmonary Delivery: Development and in vivo evaluation of dry powder inhaler. J. Pharm. Biomed. Anal., 2017, 145, 854-859.
[http://dx.doi.org/10.1016/j.jpba.2017.07.051] [PMID: 28826144]
[111]
Tang, J.; Li, J.; Li, G.; Zhang, H.; Wang, L.; Li, D.; Ding, J. Spermidine-mediated poly(lactic-co-glycolic acid) nanoparticles containing fluorofenidone for the treatment of idiopathic pulmonary fibrosis. Int. J. Nanomedicine, 2017, 12, 6687-6704.
[http://dx.doi.org/10.2147/IJN.S140569] [PMID: 28932114]
[112]
Semete, B.; Booysen, L.; Lemmer, Y.; Kalombo, L.; Katata, L.; Verschoor, J.; Swai, H.S. In vivo evaluation of the biodistribution and safety of PLGA nanoparticles as drug delivery systems. Nanomedicine (Lond.), 2010, 6(5), 662-671.
[http://dx.doi.org/10.1016/j.nano.2010.02.002] [PMID: 20230912]
[113]
Casciaro, B.; d’Angelo, I.; Zhang, X.; Loffredo, M.R.; Conte, G.; Cappiello, F.; Quaglia, F.; Di, Y.P.; Ungaro, F.; Mangoni, M.L. Poly(lactide- co-glycolide) nanoparticles for prolonged therapeutic efficacy of esculentin-1a-derived antimicrobial peptides against pseudomonas aeruginosa lung infection: in vitro and in vivo studies. Biomacromolecules, 2019, 20(5), 1876-1888.
[http://dx.doi.org/10.1021/acs.biomac.8b01829] [PMID: 31013061]
[114]
Subedi, D.; Vijay, A.K.; Willcox, M. Overview of mechanisms of antibiotic resistance in Pseudomonas aeruginosa: an ocular perspective. Clin. Exp. Optom., 2018, 101(2), 162-171.
[http://dx.doi.org/10.1111/cxo.12621] [PMID: 29044738]
[115]
Casciaro, B.; Dutta, D.; Loffredo, M.R.; Marcheggiani, S.; McDermott, A.M.; Willcox, M.D.; Mangoni, M.L. Esculentin-1a derived peptides kill Pseudomonas aeruginosa biofilm on soft contact lenses and retain antibacterial activity upon immobilization to the lens surface. Biopolymers, 2017, 110(5), e23074
[http://dx.doi.org/10.1002/bip.23074] [PMID: 29086910]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 27
ISSUE: 9
Year: 2020
Published on: 26 March, 2020
Page: [1405 - 1419]
Pages: 15
DOI: 10.2174/0929867326666190722095408
Price: $65

Article Metrics

PDF: 29
HTML: 7
EPUB: 1
PRC: 1